Coronavirus disease 2019 (COVID-19) is a respiratory illness caused by severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2). The data reported in November 2023 revealed that over 700 million people have been infected with the virus (World Health Organization, 2023). The appearance of mutations and variants of concern has caused several additional waves of infection and compromise the effectiveness of existing vaccines and antiviral drugs (Harvey et al., 2021). Moreover, SARS-CoV-2 infection has shown to cause long-term effects on human health, although the mechanisms are still poorly described (Crook et al., 2021). Even though most COVID-19 cases are mild, disease can be severe, resulting in hospitalization, respiratory failure, or even death (World Health Organization, 2023). Therefore, a remarkable feature of SARS-CoV-2 infection is the great variability in clinical phenotype among infected people. Many factors can correlate with COVID-19 disease severity, including age, gender, body mass index, previous comorbidities, immune responses, and genetics (Yang et al., 2020; Ellinghaus et al., 2020; Bastard et al., 2020). Of note, and unfortunately, the determinants of infection outcome and the pathogenic mechanisms are not completely understood yet.

SARS-CoV-2 primarily infects the respiratory tract by binding to angiotensin-converting enzyme 2 (ACE2) receptor (Zhou et al., 2020b). However, a growing body of evidence suggests that SARS-CoV-2 can also infect other organs since viral particles and nucleic acids have been found in different biological samples, like sputum, bronchoalveolar lavage fluid, faeces, blood, and urine (Peng et al., 2020; Sun et al., 2020). Thus, studies employing single-cell RNA sequencing have demonstrated that ACE2 is present in various organs and tissues, including the gastrointestinal tract, where ACE2 receptors have been reported to be highly expressed (Zhang et al., 2020). This supports several lines of evidence suggesting a substantial involvement of the gastrointestinal tract in the pathogenesis of the disease, including the ability of SARS-CoV-2 to infect and replicate in intestinal enterocytes (Lamers et al., 2020), or to increase expression of the viral entry receptor (ACE2 receptor) and several membrane-bound serine proteases (such as transmembrane protease serine 2 [TMPRSS2] and TMPRSS4) in intestinal epithelial cells (Zang et al., 2020).

In addition, reports have shown that SARS-CoV-2 infection can disrupt nasopharyngeal and intestinal microbiota composition and promote dysbiosis, reducing diversity and increasing the presence of opportunistic pathogens, including Staphylococcus, Corynebacterium, and Acinetobacter bacteria (Candel et al., 2023; Ancona et al., 2023), which can make patients more susceptible to secondary infections, rising morbidity and mortality (De Bruyn et al., 2022). Besides local changes in the respiratory tract, alterations in the distal gut microbiota have also been observed in SARS-CoV-2 infection (Gu et al., 2020; Zuo et al., 2020; Wu et al., 2021; Cao et al., 2021). Previous studies have evidenced a relevant connection between the microbiome in the nasopharynx and the gut, and preliminary data have suggested a bidirectional interaction that could play a role in the development of the immune response both in healthy and pathological conditions, including SARS-CoV-2 infection (Mancabelli et al., 2023). In this sense, dysbiosis has been associated not only with the severity of the disease but also with the recovery processes (Candel et al., 2023; Cao et al., 2021); however, little is understood of the link with the establishment of different symptomatic profiles in this condition, and to date, few studies have focused on the association between COVID-19 severity and the nasopharyngeal and faecal microbiota, being examined simultaneously.

Considering that the efficacy of the COVID-19 vaccines and antiviral drugs against SARS-CoV-2 is compromised with the emergence of mutations and new variants of the virus (Harvey et al., 2021), new therapeutic approaches and prognostic tools are still necessary. Therefore, the characterization of the nasopharyngeal and intestinal microbiome will allow to identify predictive biomarkers for the diagnosis and prognosis of the disease, as well as possible therapeutic targets in the management of SARS-CoV-2.

Recent findings have evidenced the prominent role of the microbiome in several diseases, including those caused by viruses, proving that commensal microbiota could either enhance or hinder viral infections (Mutlu et al., 2014; Guo et al., 2023). A large body of evidence indicates that respiratory virus infections can induce a microbial imbalance in the airways, increasing the risk of secondary bacterial infections and worsening the prognosis (Li et al., 2023). Besides, alterations in the gut microbiota have also been noted during respiratory virus infections, likely influenced by the ‘gut-lung axis’ (Budden et al., 2017). In this regard, different studies have tried to establish relationships between microbiota composition and SARS-CoV-2 infection (Yamamoto et al., 2021; Di Stadio et al., 2020) but just a few have explored microbiota compositional variations among patients with different symptomatology (Nguyen et al., 2023). However, only a few studies have explored the nasopharyngeal-faecal axis as a potential biomarker of severity in patients infected with SARS-CoV-2. Hence, the present study provides some biomarkers located in nasopharyngeal and gut microbiota that could help to predict COVID-19 severity.

In this context, 106 patients with SARS-CoV-2 infection were included in this study and classified into three severity groups according to their symptoms. To ensure results were derived only from SARS-CoV-2 infection, included patients were not positive for other viral infections. Considering clinical parameters, the current study confirmed that age and gender are positively associated with more severe symptoms like dyspnoea, increased heart, and respiratory rates together with lower oxygen saturation. Results that are in line with other COVID-19 studies conducted globally have shown that men and women are disproportionately affected. Data revealed that males suffered from more severe disease than females, including higher ICU admission rates, dyspnoea, increased heart rate, being all clinical signs for higher severity of the COVID-19 disease (Pijls et al., 2022; Mauvais-Jarvis, 2020). Regarding some biochemical parameters those groups of patients with moderate or severe symptoms showed significantly increased levels of D-dimer, ferritin, and CRP, which are typically described as biomarkers for COVID-19 severity (Gómez-Pastora et al., 2020; Rostami and Mansouritorghabeh, 2020; Zhou et al., 2020a). Interestingly, previous studies have reported that alterations in the gut microbiota composition in COVID-19 patients could be also associated with disease severity, measured with the elevated concentration of the blood markers described above (Liu et al., 2022a; Liu et al., 2022b; Yeoh et al., 2021). In this sense, we have confirmed these results in our study as specific bacteria from severe condition positively correlate with the levels of ferritin, CRP, D-dimer, or lymphocytes. Consequently, the microbiota could be key in the clinical phenotype of COVID-19 patients, although its specific contribution to the progression of the infection and a poor prognosis needs to be better understood.

The results of alpha diversity revealed only substantial changes in richness in the nasopharyngeal microbiome associated with moderate and severe symptoms. Although most of the studies have proposed that SARS-CoV-2 infection is associated with lower microbial diversity in nasopharyngeal samples (Candel et al., 2023; Gao et al., 2021; Gupta et al., 2022), others did not find differences in alpha diversity composition among groups with different symptomatology (De Maio et al., 2020; Braun et al., 2021). This could be explained by the diverse methods of sample collection, and also the SARS-CoV-2 variant and the treatment with antibiotics (Bose et al., 2023).

Furthermore, in the present study, beta diversity analysis showed that in both types of samples every group of patients presented distinctly differentiated clusters. As previously reported, COVID-19 disease severity is more dependent on the presence or absence of certain bacteria rather than alterations in bacterial diversity and richness (Wang et al., 2023). This argument was supported by the characterization of bacterial microbiota composition at phyla and genera levels. In nasopharyngeal swabs, the abundance of Bacteroidota and Actinobacteriota was reduced compared to mild patients, which goes in accordance with previous reports where these bacteria have been previously linked to a better prognosis of SARS-CoV-2 infection since it can exert beneficial effects by preventing respiratory diseases, including COVID-19 (Nardelli et al., 2022; Bozkurt and Bilen, 2021; Wei et al., 2023; Bassis et al., 2014; Pérez-Losada et al., 2023). Moreover, the abundance of Bacillota and Pesudomonadota was increased in patients with severe symptomatology, thus supporting previous studies in which higher counts of Bacillota (Staphylococcus sp. and Streptococcus sp.) and Pesudomonadota (Pseudomonas sp.) were associated with moderate and severe symptoms of COVID-19 (Garcia-Vidal et al., 2021).

Regarding genera composition, Alistipes and Muribaculaceae were highly abundant in patients with mild symptoms. These bacteria have been well characterized in gut microbiota, but little is known about their presence in nasopharyngeal microbiota. Different experimental studies in mice have suggested their role in viral infections. Thus, Muribaculaceae was found in the lung microbiota in SARS-CoV-2-infected mice that were treated with a selective inhibitor of the main protease (M^pro) (Seibert et al., 2021). In the case of Alistipes, in a study conducted in children infected with respiratory syncytial virus (RVS), its abundance was reduced in the nasopharyngeal microbiota in comparison with non infected subjects (Schippa et al., 2020). Overall, these genera could be associated with a protective role against viral infection, and their higher presence in nasopharyngeal samples from mild COVID-19 patients could prevent the progression to severe disease.

In contrast, the increased presence of other genera, such as Corynebacterium, Acinetobacter, Staphylococcus, and Veillonella, was associated with the severity of SARS-CoV-2 infection. This is supported by previous studies in which these genera were associated with both disease severity and systemic inflammation (Ma et al., 2021). In addition, higher abundance of Enterococcus was observed in severe patients, thus confirming other studies in critically ill patients (Merenstein et al., 2021).

On the contrary, findings at phylum level in stool samples did not reveal notable modifications among patient groups. However, in mild ill patients, different genera from Clostridia class (Clostridia, Coprococcus, Dorea, Lachnospiraceae, Roseburia, and Ruminococcus) and Barnesiella were identified as highly abundant. While the class Clostridia was associated with a reduced production of proinflammatory cytokines in COVID-19 patients and in those who recovered from the infection (Mizutani et al., 2022; Mańkowska-Wierzbicka et al., 2023), Barnesiella prevents colonization by antibiotic-resistant bacteria such as Enterococcus, which has been reported as a frequent cause of systemic infection in critically ill COVID-19 patients (Ubeda et al., 2013; Giacobbe et al., 2021). Thus, the reduction of gut abundance of Barnesiella and Clostridia members could be associated with more severe symptoms in COVID-19 patients. Moreover, the specific genera detected in the severe illness group, Lachnocostridum, Anaerococcus, and Peptoniphilus, have been previously recognized as opportunistic pathogens, which could induce gut inflammation and contribute to a poor prognosis (Murphy and Frick, 2013).

Considering the variations observed in both nasopharyngeal and gut microbiota composition and their miscellaneous effects, the identification of specific bacteria could be used as a biomarker to predict COVID-19 severity. Accordingly, the present study has identified unique ASVs for the different severities of COVID-19. For nasopharyngeal samples, species belonging to the genus Lactobacillus (L. fermentum or L. reuteri) or Prevotella (P. pallens, P. ori, and P. shahii) have been pinpointed. Interestingly, mild patients have also shown a higher content of Lactobacillus, which could also contribute to the host defence against viral infection at early stages, as reported in asymptomatic COVID-19 patients (Kageyama et al., 2022). In the case of Prevotella sp., its role in COVID-19 infection has not been clearly elucidated, but previously published microbiome analysis has revealed that its abundance was higher in mild patients (Chen et al., 2022). Nevertheless, others have suggested that it could be a biomarker of critical phenotype in COVID-19 patients (Haran et al., 2021; Lu et al., 2023). It is interesting to highlight that Anaerococcus prevotii was one of the species exclusively found in stools in mild patients. This microorganism has already been linked to lower inflammation in COVID-19 patients (Seong et al., 2023). Conversely, Coprobacillus cateniformis was only found in severe patients, and could be involved in the development of a worse condition in these patients through ACE2 upregulation (Zuo et al., 2020).

Even though these bacteria were found to be unique for each group, LEfSe was performed to obtain specific severity prognostic biomarkers depending on the abundance threshold. Therefore, for mild patients, Burkholderia and Paraburkholderia were identified in nasopharyngeal swabs and B. coprocola and R. bicirculans in stool samples. Although the information regarding the first two species in humans is limited, a few studies have reported their presence in the commensal human microbiota (Ning et al., 2022; Mengyi et al., 2023). Contrarily, B. coprocola and R. bicirculans have been found in both healthy and COVID-19 patients, being the abundance of R. bicirculans reduced in infected subjects (Li et al., 2021).

Correspondingly, in patients with moderate symptoms, P. veronii was detected in nasopharyngeal samples whereas P. stercorea, B. cellulosilyficus, B. stercoris, and P. copri were identified in stool samples. In general, these findings agree with previous studies (de Nies et al., 2023). Xu et al. found that infected patients showed higher abundance of B. cellulosilyficus (Xu et al., 2022), whereas B. stercoris and P. copri were associated with ACE2 upregulation and increased proinflammatory cytokine production, respectively, in COVID-19 patients (Li et al., 2021; Lymberopoulos et al., 2022).

Likewise, in critically ill patients, the biomarkers detected for nasopharyngeal microbiota were M. salivarium, P. dentalis, Leptotrichia, and H. parainfluenzae, while, in stool samples, Escherichia sp., E. durans, A. Onderdonkii, P. timonensis, and P. bivia were the species recognized as biomarkers. Both P. bivia and P. timonensis have been defined as unique microorganisms in COVID-19 patients’ microbiota (Li et al., 2021; Thissen et al., 2022), whilst a higher abundance of M. salivarium, H. parainfluenzae, and E. durans were related to poor prognosis (Sulaiman et al., 2021; Devi et al., 2023; DeVoe et al., 2022). When considering A. onderdonkii, it is a short-chain fatty acid-producing bacteria that has been reported to be inversely associated with COVID-19 severity (Zuo et al., 2020; Wang et al., 2023); however, there is conflicting evidence regarding its pathogenicity that indicates that A. onderdonkii may have protective effects against some diseases, including COVID-19 (Zuo et al., 2020). Nonetheless, considering that Zuo et al. employed a different methodology to analyse microbiota composition from stool samples, A. onderdonkii could be considered as a biomarker of severe condition in SARS-CoV-2-infected subjects.

Of note, the use of these bacteria as biomarkers of severity in SARS-CoV-2 infection is further supported by the fact that these species exhibited positive correlations with critical clinical variables mentioned above. Specifically, possible severe biomarkers from nasopharyngeal samples such as M. salivarium, H. parainfluenzae, and P. dentalis showed a negative correlation towards lymphocytes count. This also happens for stool severe biomarkers P. bivia and P. timonensis. As it is well established that microbiota can modify blood cells count (Khosravi et al., 2014), it would not be a surprise that these bacteria could promote COVID-19 severity by lowering lymphocyte count. In addition, P. bivia and P. timonensis showed positive correlation with ferritin, CRP, and D-dimer levels, as well as cardiomyopathy and respiratory rates. Several studies have revealed both the relationship between CRP levels, gut microbiota, and COVID-19 severity (Moreira-Rosário et al., 2021), as well as the positive correlation of specific bacteria with D-dimer, CRP, and the levels of pro-inflammatory mediators in plasma (Zhou et al., 2021).

Finally, although the composition of the nasal and faecal microbiota in COVID-19 patients has been previously studied (Li et al., 2023), the interaction between these microbiotas has not been extensively evaluated. In this study, we analysed the relationship between specific bacteria from nasopharyngeal and stool samples, confirming a correlation between the abundances of species in these different sample types. Concretely, a strong positive correlation between P. timonensis (in stool samples) towards P. dentalis and M. salivarium (in nasopharyngeal samples) was found in severe patients. To maximize the potential use of these biomarkers, the ratio of the abundance of these species was also significantly increased within the highest severity of this condition. As a result, the ratio proposed in this study could be used as a novel predictor to identify critically ill COVID-19 patients as the ratio Bacillota and Bacteroidetes has been used as a marker of dysbiosis (Ley et al., 2006). In this case, the ratio P. timonensis/P. dentalis and P. timonensis/M. Salivarium could be a prognostic tool for severe SARS-CoV-2, and its increase could be associated with a higher risk COVID-19 severity development.

Sequencing data have been deposited in Harvard Database (16S DNA sequences from stool samples of patients infected by SARS-CoV-2). Code is available in a GitHub repository (https://github.com/albarodnog/COVID-INMUNOBIOTICS-Group copy archived at Rodríguez Nogales, 2024).

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Author details

1. Benita Martin-Castaño

   1. Centro de Salud Las Gabias, Distrito Granada-Metropolitano, Granada, Spain
   2. Instituto de Investigación Biosanitaria de Granada (ibs.GRANADA), Granada, Spain

   Contribution

   Conceptualization, Investigation, Methodology

   Contributed equally with

   Patricia Diez-Echave

   Competing interests

   No competing interests declared

2. Patricia Diez-Echave

   1. Instituto de Investigación Biosanitaria de Granada (ibs.GRANADA), Granada, Spain
   2. Department of Pharmacology, Center for Biomedical Research (CIBM), University of Granada, Granada, Spain

   Contribution

   Investigation, Methodology

   Contributed equally with

   Benita Martin-Castaño

   Competing interests

   No competing interests declared

3. Jorge García-García

   1. Instituto de Investigación Biosanitaria de Granada (ibs.GRANADA), Granada, Spain
   2. Department of Pharmacology, Center for Biomedical Research (CIBM), University of Granada, Granada, Spain
   3. Servicio Microbiología, Hospital Universitario Clínico San Cecilio, Granada, Spain

   Contribution

   Data curation, Software, Formal analysis, Investigation, Methodology, Writing – original draft, Writing – review and editing

   For correspondence

   jgar11gar@gmail.com

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0003-0925-9441

4. Laura Hidalgo-García

   1. Instituto de Investigación Biosanitaria de Granada (ibs.GRANADA), Granada, Spain
   2. Department of Pharmacology, Center for Biomedical Research (CIBM), University of Granada, Granada, Spain

   Contribution

   Investigation, Methodology

   Competing interests

   No competing interests declared

5. Antonio Jesús Ruiz-Malagon

   1. Instituto de Investigación Biosanitaria de Granada (ibs.GRANADA), Granada, Spain
   2. Department of Pharmacology, Center for Biomedical Research (CIBM), University of Granada, Granada, Spain

   Contribution

   Investigation, Methodology

   Competing interests

   No competing interests declared

6. José Alberto Molina-Tijeras

   1. Instituto de Investigación Biosanitaria de Granada (ibs.GRANADA), Granada, Spain
   2. Department of Pharmacology, Center for Biomedical Research (CIBM), University of Granada, Granada, Spain

   Contribution

   Investigation, Methodology

   Competing interests

   No competing interests declared

7. María Jesús Rodríguez-Sojo

   1. Instituto de Investigación Biosanitaria de Granada (ibs.GRANADA), Granada, Spain
   2. Department of Pharmacology, Center for Biomedical Research (CIBM), University of Granada, Granada, Spain

   Contribution

   Investigation, Methodology

   Competing interests

   No competing interests declared

8. Anaïs Redruello-Romero

   Instituto de Investigación Biosanitaria de Granada (ibs.GRANADA), Granada, Spain

   Contribution

   Methodology

   Competing interests

   No competing interests declared

9. Margarita Martínez-Zaldívar

   1. Instituto de Investigación Biosanitaria de Granada (ibs.GRANADA), Granada, Spain
   2. Centro de Salud “Salvador Caballero”, Distrito Granada-Metropolitano, Granada, Spain

   Contribution

   Resources, Data curation

   Competing interests

   No competing interests declared

10. Emilio Mota

    Centro de Salud “Salvador Caballero”, Distrito Granada-Metropolitano, Granada, Spain

    Contribution

    Data curation

    Competing interests

    No competing interests declared

11. Fernando Cobo

    Servicio Microbiología, Hospital Universitario Virgen de las Nieves, Granada, Spain

    Contribution

    Data curation

    Competing interests

    No competing interests declared

12. Xando Díaz-Villamarin

    Instituto de Investigación Biosanitaria, Granada, Spain

    Contribution

    Investigation

    Competing interests

    No competing interests declared

    "This ORCID iD identifies the author of this article:" 0000-0003-0849-9902

13. Marta Alvarez-Estevez

    1. Instituto de Investigación Biosanitaria de Granada (ibs.GRANADA), Granada, Spain
    2. Servicio Microbiología, Hospital Universitario Clínico San Cecilio, Granada, Spain
    3. CIBER de Enfermedades Infecciosas (CIBER-Infecc), Instituto de Salud Carlos III, Madrid, Spain

    Contribution

    Investigation

    Competing interests

    No competing interests declared

14. Federico García

    1. Instituto de Investigación Biosanitaria de Granada (ibs.GRANADA), Granada, Spain
    2. Servicio Microbiología, Hospital Universitario Clínico San Cecilio, Granada, Spain
    3. CIBER de Enfermedades Infecciosas (CIBER-Infecc), Instituto de Salud Carlos III, Madrid, Spain

    Contribution

    Resources, Investigation

    Competing interests

    No competing interests declared

15. Concepción Morales-García

    Respiratory Medicine Department, Hospital Universitario Virgen de las Nieves, Granada, Spain

    Contribution

    Investigation

    Competing interests

    No competing interests declared

16. Silvia Merlos

    Respiratory Medicine Department, Hospital Universitario Virgen de las Nieves, Granada, Spain

    Contribution

    Investigation

    Competing interests

    No competing interests declared

17. Paula Garcia-Flores

    Respiratory Medicine Department, Hospital Universitario Virgen de las Nieves, Granada, Spain

    Contribution

    Investigation

    Competing interests

    No competing interests declared

18. Manuel Colmenero-Ruiz

    1. Instituto de Investigación Biosanitaria de Granada (ibs.GRANADA), Granada, Spain
    2. Servicio de Medicina Intensiva, Hospital Universitario Clínico San Cecilio, Granada, Spain

    Contribution

    Resources, Investigation

    Competing interests

    No competing interests declared

19. José Hernández-Quero

    1. Instituto de Investigación Biosanitaria de Granada (ibs.GRANADA), Granada, Spain
    2. Servicio de Enfermedades Infecciosas, Hospital Universitario Clínico San Cecilio, Granada, Spain

    Contribution

    Investigation

    Competing interests

    No competing interests declared

20. Maria Nuñez

    1. Instituto de Investigación Biosanitaria de Granada (ibs.GRANADA), Granada, Spain
    2. Servicio Farmacia Hospitalaria, Hospital Universitario Clínico San Cecilio, Granada, Spain
    3. CIBER de Epidemiología y Salud Pública (CIBER-ESP), Instituto de Salud Carlos III, Madrid, Spain

    Contribution

    Investigation

    Competing interests

    No competing interests declared

21. Maria Elena Rodriguez-Cabezas

    1. Instituto de Investigación Biosanitaria de Granada (ibs.GRANADA), Granada, Spain
    2. Department of Pharmacology, Center for Biomedical Research (CIBM), University of Granada, Granada, Spain

    Contribution

    Investigation, Writing – review and editing

    Competing interests

    No competing interests declared

22. Angel Carazo

    1. Instituto de Investigación Biosanitaria de Granada (ibs.GRANADA), Granada, Spain
    2. Servicio Microbiología, Hospital Universitario Clínico San Cecilio, Granada, Spain

    Contribution

    Validation, Investigation

    Competing interests

    No competing interests declared

23. Javier Martin

    Department of Cell Biology and Immunology, Institute of Parasitology and Biomedicine López-Neyra, CSIC, Granada, Spain

    Contribution

    Validation, Investigation

    Competing interests

    No competing interests declared

24. Rocio Moron

    1. Instituto de Investigación Biosanitaria de Granada (ibs.GRANADA), Granada, Spain
    2. Servicio Farmacia Hospitalaria, Hospital Universitario Clínico San Cecilio, Granada, Spain

    Contribution

    Formal analysis, Supervision, Validation, Investigation, Methodology, Writing – original draft, Writing – review and editing

    For correspondence

    rmoronr@gmail.com

    Competing interests

    No competing interests declared

25. Alba Rodríguez Nogales

    1. Instituto de Investigación Biosanitaria de Granada (ibs.GRANADA), Granada, Spain
    2. Department of Pharmacology, Center for Biomedical Research (CIBM), University of Granada, Granada, Spain

    Contribution

    Formal analysis, Supervision, Validation, Investigation, Writing – original draft, Writing – review and editing

    Contributed equally with

    Julio Galvez

    Competing interests

    No competing interests declared

    "This ORCID iD identifies the author of this article:" 0000-0003-1927-0628

26. Julio Galvez

    1. Instituto de Investigación Biosanitaria de Granada (ibs.GRANADA), Granada, Spain
    2. Department of Pharmacology, Center for Biomedical Research (CIBM), University of Granada, Granada, Spain
    3. CIBER de Enfermedades Hepáticas y Digestivas (CIBER-EHD), Instituto de Salud Carlos III, Madrid, Spain

    Contribution

    Conceptualization, Resources, Formal analysis, Supervision, Funding acquisition, Validation, Visualization, Writing – original draft, Writing – review and editing

    Contributed equally with

    Alba Rodríguez Nogales

    Competing interests

    No competing interests declared

    "This ORCID iD identifies the author of this article:" 0000-0001-6876-3782

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